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Aug 12, 2017 - P-rich bottom water can be injected into photic zone during wind-driven mixing and overturn of the water column, al- though its frequency and ...
Environ Sci Pollut Res (2017) 24:21509–21516 DOI 10.1007/s11356-017-9931-3

SHORT RESEARCH AND DISCUSSION ARTICLE

Sediment lipid biomarkers record phytoplankton dynamics of Lake Heihai (Yunnan Province, SW China) driven by climate warming since the 1980s Yongdong Zhang 1 & Yaling Su 1 & Zhengwen Liu 1,2 & Jinlei Yu 1 & Miao Jin 1

Received: 27 November 2016 / Accepted: 7 August 2017 / Published online: 12 August 2017 # Springer-Verlag GmbH Germany 2017

Abstract Increased phosphorus (P) export from sediments to the overlying water column is a significant factor driving the variation of phytoplankton in productivity and community structure in lakes. However, the lack of long-term instrumental data often impeded analyses attempting to associate dynamics of phytoplankton with variation of internal P loading. Here, elements and lipid biomarkers were analyzed in a sediment core from Lake Heihai, a small, deep, and ultraoligotrophic alpine lake in Haba Mountain, Yunnan Province, SW China. The data document incredible enrichment of element iron (Fe) in the sediment, whose concentrations are much higher than those of other common major elements including titanium (Ti), aluminum (Al), calcium (Ca), and magnesium (Mg). This finding, together with the abundance correlation between P and Fe (n = 30, R2 = 0.783) suggested that P was probably retained in sediments through sorption with micro-layer of FeOOH at the sediment-water interface. The P/Ti ratios, P/ Fe ratios, and P/total organic carbon (TOC) ratios all declined in the sediment since 1980, perhaps indicating increased P release from sediments to the overlying water column initiated by hypolimnion anoxia and sulfidic, which is presumably triggered by regional climate warming since the 1980s. The Responsible editor: Boqiang Qin * Yongdong Zhang [email protected] * Zhengwen Liu [email protected]

1

State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography & Limnology, Chinese Academy of Sciences, Nanjing 210008, China

2

Department of Ecology and Research Center of Hydrobiology, Jinan University, Guangzhou 510632, China

P-rich bottom water can be injected into photic zone during wind-driven mixing and overturn of the water column, although its frequency and intensity might decline due to stronger water column stratification in warming climate. In response, diatoms exhibited a rapid increase of productivity at this time, because diatoms have a storage vacuole and thereby nutrients such as P can be concentrated and used for cell division long after they are depleted in the bulk fluid. Elevated diatom biomass produced shading of light penetration, allowing for a low productivity for dinoflagellates. This study deepens our understanding of the impact of climate warming on lake systems and highlights the element biogeochemical cycle contributing to the variation of nutrients in the lake water column. Keywords Lipid biomarker . Fe and P . Alpine lake . Geochemical . Sediment

Introduction Lake biota can exhibit a clear response to climate-driven changes in lake environment, either directly (temperature and light penetration) or indirectly (nutrients) (Korhola et al., 2002; Sorvari et al., 2002). For example, climate-dependent water column stratification is known to strongly affect the light, nutrient, oxygen, and pH regime that planktonic organisms experience. During warming period, stable water column stratification developed, which may have created favorable condition for the growth of plankton (Sorvari et al., 2002). However, a strong water column stratification has been reported to impede nutrient recharge from hypolimnion to photic zone and thus reduce phytoplankton productivity (Tierney et al., 2010). In addition, the hypolimnion could turn to be anoxic and sulfidic when a lake had strong thermal

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stratification and experienced significant terrestrial organic matter (OM) loading in warming climate (Zhang et al., 2016b). These prominent changes in water environment might trigger P release from sediments to the hypolimnion because solid FeOOH-PO4 complexes dissolved when they reacted with sulfidic (Cappellen and Ingall, 1994; McManus et al., 1997), and the elevated regenerating P may have further altered phytoplankton productivity (Filippelli et al., 2003; Kuypers et al., 2004; Mort et al., 2007). Unfortunately, empirical demonstrations of its existence in natural lakes remain relatively undescribed by long-term water column monitoring data or sediment geochemical records. Attempts at long-term direct monitoring of nutrients (e.g., total phosphorus, TP) and phytoplankton in lakes have been sporadic and fairly inconsistent, with detailed data only available for limited periods of time at sparsely distributed locations around the world. Generally, the remote alpine lakes had little monitoring data because these lakes are beyond the areas for human activities. However, these lakes provide a valuable site for studying the relation between phytoplankton dynamics and climate variation due to the lack of human activities in the catchment. Fortunately, sediment geochemical records can be used to reconstruct past variations of environment and ecosystem in lakes. The extent of P retained in sediments reflects a variation of P in the overlying water, and/or the variation of iron content, and redox condition in the sediment (Smol, 2008). During hypolimnion anoxia, however, sediment P might be anticorrelated with water column P (Last and Smol, 2001). The biogenic specificity and relative simple diagenetic transformation of certain lipid compounds found in lake sediments render them useful as biomarkers, allowing for inferring the historic variations of phytoplankton productivity and community structures (Meyers, 2003; Lu and Meyers, 2009). It is widely accepted that dinosterol and 24methylenecholesterol in sediments are associated with dinoflagellates and diatoms inputs from the overlying water column (Volkman et al., 1998). Lake Heihai is a small alpine lake in Yunnan Province, SW China. The lake was rarely disturbed by human activities due to its high altitude, and the temperature around the lake had a quick increase since the 1980s (Zhang et al., 2016b). The warming climate stimulated water column stratification of the lake and thereby altered its redox cyclicity and nutrient recycling. The lake ecosystems might respond rapidly and strongly to changes in both the lake itself and its catchment area because the lake is small, with harsh meteorological and rapid flushing rates. Therefore, Lake Heihai is an ideal site for studying the response of ecosystems to environmental variation driven by climate warming. Although no water column monitoring program was conducted in this remote lake, past environment and ecosystem in the lake can be recognized indirectly from the sediment geochemical records. Here we report a sediment stratigraphic variation of lipid biomarkers

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and lithogenic elements in Lake Heihai that describes the pattern of response of phytoplankton ecosystem to regional climate warming.

Materials and methods Lake Heihai is located at 4118 m a.s.l. in Haba Mountain (Fig. 1a). The lake is small (~ 0.18 km2) and deep (Zmax = 42 m, Zmean = 22.2 m), with a steep-sided morphometry and a high catchment: lake ratio (~ 9). The lake water currently has total nitrogen (TN) of 0.21 mg/L, TP of 0.006 mg/L, chlorophyll a (Chla) of 0.5 μg/L, and a Secchi depth (SD) of 4.5 m. Zhongdian climate station, the nearest monitoring station to Lake Heihai (~ 35 km), recorded a quick increase of temperature in this area since the 1980s (Fig. 1c) (Zhang et al., 2016b). In October 2012, a sediment core (HH-1 core) with lengths of 30 cm was collected from the center of the lake using an UWITEC gravity corer. The core was sub-sampled at 1-cm contiguous intervals and refrigerated at −20 °C prior to geochemical and chronology analysis. Chronology of the HH-1 core (Fig. 1b) was previously established by the decay profile of unsupported 210Pb activity and the constant rate of supply (CRS) model (Zhang et al., 2016b). Geochemical analysis of the sediments was described in detail from previous publication (Zhang et al., 2016b). In brief, TOC and TN in the sediments were determined by a CHNS Vario E1 III elemental analyzer after removing carbonate. Major and trace elements (including Fe, Al, Ti, Mg, Ca, manganese (Mn), and P) in the samples were determined by inductively coupled plasma– atomic emission spectrometry (ICP–AES), and inductively coupled plasma–mass spectrometry (ICP–MS) after the sediments were nitrified by HNO3, HCL and HF and dissolved in HCLO4. Lipid biomarkers in the sediments were acquired by Soxhlet extraction using dichloromethane/methanol (9:1 v/v) as solvent. The n-alkanol/sterol fraction was separated from other fractions by column chromatography and measured by gas chromatography–mass spectrometry (GC–MS) after derivatization with N,O-bis(trimethylsilyl)trifluoroacetamide. Compounds were identified by comparing with previously reported mass spectra, and by interpretation of fragmentation patterns and chromatographic retention behavior. Quantification data was determined by comparing peak areas of the internal standard with compounds of interest in reconstructed total ion current (TIC) chromatograms.

Results The major element fraction in the sediment of the HH-1 core contained abundant Fe (89.3–135.6 mg g−1) and relatively less Ti, Al, Ca, and Mg, resulting in high levels of Fe/Ti ratios (8.55– 18.66), Fe/Al ratios (1.52–2.86), Fe/Ca ratios (5.00–10.12), and

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Fig. 1 a Map showing the location of the study site (Lake Heihai in Haba Mountain), b CRS-modeled age-depth plot in the HH-1 core, and c temperature variation around Lake Heihai since the 1950s

Fe/Mg ratios (1.11–2.26) (Fig. 2a–e). Moving up the core, from older deeper sediments to more recent ones, especially after 1980, P/Fe ratios (0.02–0.04), P/Ti ratios (0.19–0.77), and P/ TOC ratios (0.08–0.26) declined markedly over time (Fig. 2a, f). In addition, Fe and P exhibited similar trends in abundance through the core (Fig. 3a), and a high degree of correlation was found between the two elements (R2 = 0.783, n = 30). A negative abundance correlation was found between P and Ca (Fig. 3c), and no correlation was established between abundances of P and TOC (or Mn) (Fig. 3b, d).

Short-chain n-alkanol abundances (sum of n-C14 + n-C16 + n-C18 + n-C20 alkanol) varied from 332.6 to 704.2 μg g−1 TOC, with notably high values in the sediment since 1980 (Fig. 4a). 24-Methylenecholesterol (24-methylcholesta5,24(28)-dien-3β-ol, C28 Δ5,24(28)) and brassicasterol (24methylcholesta-5,22-dien-3β-ol, C28 Δ5,22) had similar trends in abundance, with levels varying from 18.6 to 82.4 μg g−1 TOC and from 52.4 to 245.7 μg g−1 TOC, respectively in the core (Fig. 4b). Elevated values were recorded in the sediment since 1980 (Fig. 4b). In contrast, dinosterol (4α,23,24-

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Fig. 2 Vertical profiles of element abundances and ratios in the core

trimethyl-5α-cholest-22E-en-3β-ol, C30 Δ22) abundances (30.9–59.7 μg g−1 TOC) slightly declined at this time (Fig.

4a). Dinosterol/24-methylenecholesterol ratios (0.57–2.43) and dinosterol/brassicasterol ratios (0.19–0.91) followed

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Fig. 3 The abundance correlation between P and Fe, Ca, Mn, and TOC

similar trends through the core, with lower values in the sediment since 1980 (Fig. 4c).

Discussion Short-chain n-alkanols are regarded as less accurate indicators of biotic sources owing to their ubiquitous in phytoplankton (Pearson et al., 2007). Conversely, dinosterol and 24methylenecholesterol are exclusively produced by dinoflagellates and diatoms, respectively (Volkman et al., 1998; Rampen et al., 2010). Brassicasterol in lake sediments is derived mainly from diatoms (Schubert et al., 1998; Zhang et al., 2016a). The similar variation between brassicasterol and 24methylenecholesterol (Fig. 4b) suggested that both of them can represent OM input from diatoms. In the current study, we found the abundance pattern of dinosterol (Fig. 4a) was against with the expected variation during OM diagenesis and concluded that the other two sterols were not significantly influenced by diagenesis process on their abundances, because these sterols and dinosterol had similar response to OM diagenesis (Zimmerman and Canuel, 2002). Rather, sterol abundance in the sediment is mainly representative of algal OM input from the overlying water column that further

reflects past algal productivity. The sterol variation in abundance in the current sediment core indicated a rapidly elevated diatom productivity and a slightly reduced dinoflagellate productivity since 1980. The algal structure at this time, as indicated by dinosterol/24-methylenecholesterol ratios and dinosterol/brassicasterol ratios (Fig. 4c), turned to be a marked increase of diatoms in percentage. These prominent paleoecological changes were commonly a response to enhanced loading of nutrients in the aquatic photic zone (Wetzel, 2001; Zimmerman and Canuel, 2002). For example, P-rich upwelling water can significantly stimulate algal productivity, especially for diatoms (Xing et al., 2016). Indeed, a substantial increase of algal productivity cannot be realized without an adequate nutrient (N and P) supply even triggered by climate warming (Bergström and Jansson, 2006). Algal productivity in Lake Heihai is dependent on P loading given the high TN/ TP ratios (> 22) in the water (Guildford and Hecky, 2000). As such, elevated P input in the photic zone of the lake can explain the observed variation of algal productivity and community structure since 1980. Anthropogenic P input has commonly placed pressure on aquatic ecosystems (Ekdahl et al., 2004). This effect should be minimal in Lake Heihai because human activities were almost absent around the lake. Variation of Ti and Al in the core (Fig. 2c, d) indicated an enhanced

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Fig. 4 Vertical profiles of biomarker abundances and ratios in the core

input of detrital materials in the lake since 1980, which generally raised P accumulation in the sediment (Zhang et al., 2016a). However, P/Ti ratios declined in the sediment at this time (Fig. 2f), reflecting a possibility of P release from sediments. Thus, increased P input from sediments to the overlying water might contribute to the eutrophication of the lake (Nikolai and Dzialowski, 2014). Sedimentary P can be categorized into three main fractions, including apatite P (Ca-P), non-apatite inorganic P (Fe-P and Mn-P) and organic P (Hiriart-Baer et al., 2011). The correlation analysis conducted between P and Ca, Fe, Mn, and TOC in the sediment suggested that P bound to Fe (Fe-P) was the major P speciation (Fig. 3). This possibility agrees with the correlation found between P levels and Fe/Ti ratios (R2 = 0.75, n = 30); the data illustrate the covariation between P and Fe levels was not caused by dilution or concentration effects of bulk sedimentation as a consequence of variation of sedimentation rate (Filippelli et al., 2003). According to the theory from Mortimer (1941, 1942), P moving between sediments and the overlying water column is controlled primarily by the content of ferric iron (FeOOH) in the sediment. Given the abnormal high abundances of Fe in the sediment of current study, P retention in sediments could be adsorbed actually onto iron oxides, such as the micro-layer of FeOOH. Variation of P in the sediment was thus controlled mainly by amounts of Fe introduced to the lake and the water column redox condition which decided iron oxide abundances in the

sediment (Ingall and Jahnke 1994; Smol, 2008; Poulton et al., 2015). Before 1980, both Fe and P exhibited a relatively high level in the sediment (Fig. 2a). The lake in this period developed seasonally hypolimnion anoxia but not turned to a sulfidic state (Zhang et al., 2016b). In anoxic, non-sulfidic and ferruginous (Fe-rich) water conditions, phosphate coprecipitation with freshly precipitated Fe (oxyhyr) oxides created a close Fe–P coupling and extensive P burial (Poulton et al., 2015). After 1980, rates of sulfate reduction elevated and thereby stimulated a sulfidic condition in hypolimnion of the lake, presumably owing to a strong water column stratification and enhanced terrestrial OM input in warming climate (Fig. 1c, Zhang et al., 2016b). The sequestered P in the sediment can be remobilized back into the overlying water column in this case, via either sulfide-promoted reduction of Fe oxides or preferential release of P from OM during bacterial sulfate reduction, and as a result, P was depleted in the sediment (Murphy et al., 2000; März et al., 2008; Poulton et al., 2015). In the sediment of current study, both P/TOC and P/ Fe declined since 1980 (Fig. 2a, f), supporting elevated P release from the sediment at this time (Ning et al., 2016). The buildup of P in the hypolimnion, and subsequent overturn driven by winds would inject P-rich bottom waters into the photic zone. The biotic response to this overturn is high productivity, particularly for diatoms (Korhola et al., 2002; Filippelli et al., 2003), because for non-motile taxa such as diatoms, nutrients are re-supplied to the bulk fluid mainly by

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turbulent mixing (Falkowski and Oliver, 2007). Diatoms have a storage vacuole in which nutrients that are taken up from the environment can be concentrated and used for cell division long after they are depleted in the bulk fluid. Storage vacuoles provide diatoms with a strong competitive advantage when nutrients are injected into the upper water column in turbulent pulses (Falkowski and Oliver, 2007). Alternatively, reduced dinoflagellate productivity could be partially caused by less light penetration because of shading by largely increased diatom concentrations under P-rich condition (Koutsodendris et al., 2015). Besides the cycling of P back into surface waters, the overturn process would introduce oxygenated waters to the benthic environment. This accounts for the modest Mo enrichment (Zhang et al., 2016b) and most importantly, provides a mechanism for phosphate to circumvent the Fe oxyhydroxide trap, which would have been present at the chemocline (Murphy et al., 2000).

Conclusion In warming climate, Lake Heihai had a strong water column stratification and received a significant loading of terrestrial OM, which fundamentally and permanently altered the lake environmental from its natural baseline. Most importantly, the sediment and hypolimnion turned to be anoxia and sulfidic, which raised P release from sediments to the overlying water column. P-rich bottom water considerably stimulated diatom productivity after they were injected into photic zone during wind-driven mixing and overturn of the water column. This is because diatoms have a storage vacuole and thereby P can be concentrated and used for cell division long after it is depleted in the bulk fluid. The diatom bloom probably suppressed dinoflagellate growth to some extent. Acknowledgements The suggestions of the reviewer and associate editor improved the manuscript greatly. Special thanks go to Prof. Kuanyi Li for discussion of this manuscript. This study was supported by the National Natural Science Foundation of China (Grant No. 41673046, 41530753 and U1033602) and B135^NIGLAS Key Program (NIGLAS2012135007).

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